The unique rectus extraocular muscles of cetaceans: Homologies and possible functions

Abstract

Each rectus extraocular muscle in cetaceans divides into two portions: a massive palpebral belly that inserts into the deep surface of the eyelids and a smaller scleral belly that inserts onto the eyeball. While the cetacean palpebral insertions have long been recognized, their homologies and functions remain unclear. To compare cetacean rectus EOM insertions with the global and orbital rectus EOM insertions of other mammals we dissected orbital contents of 20 odontocete species, 2 mysticete species and 18 non‐cetacean species, both aquatic and terrestrial. Four cetacean species were also examined with magnetic resonance imaging (MRI). All four rectus muscles in cetaceans had well‐developed palpebral bellies and insertions. Adjacent palpebral bellies showed varying degrees of fusion, from near independence to near complete fusion. Fusion was most complete towards palpebral insertions and less towards origins. A medial moiety of the superior rectus palpebral belly is likely the levator palpebrae superioris. Smaller but still robust scleral insertions were present on all recti, with the medial rectus (MR) being significantly more muscular than the others. All non‐cetacean species examined had recti with distinct global and orbital insertions, the latter generally onto Tenon's capsule. Orbital insertions in pygmy hippopotamus and Florida manatee extended into the deep surfaces of the eyelids, hence qualifying as palpebral insertions. Our results suggest that rectus EOMs of mammals generally have both global and orbital insertions, and that palpebral bellies of cetaceans and other species are modified homologs of the orbital insertions. The presence of palpebral insertions in pygmy hippopotamus and absence in other cetartiodactyls suggests an intermediate condition between terrestrial cetartiodactyls and cetaceans. Palpebral insertions in Florida manatee and reports of their presence in some pinnipeds suggest parallel evolution in multiple aquatic lineages. Various functions of cetacean palpebral recti have been proposed, including eyelid dilators, protection during diving and thermogenesis for warming eye and brain. For further insight into their possible functions, we observed eye movements of captive bottlenose dolphins (Tursiops truncatus) at the U.S. National Aquarium. Our observations showed that in addition to rotation of the eyeball the entire surrounding palpebral region also moves during gaze changes. For example during upward gaze the globe not only rotates in supraduction but translates dorsally as well. It appears the rectus palpebral bellies are responsible for flexing the palpebral structures and thus also translating the globe, while the scleral insertions act directly for ocular rotation. Along with frequent non‐conjugate eye movements, the oculomotor mechanics and repertoire of cetaceans are thus quite distinctive. Summarily, axial displacement within the orbit is a major ‘eye movement’ in cetaceans, with protrusion and retraction mediated by well‐developed circular muscles and retractor bulbi respectively. Torsional eye movements driven by elaborate oblique EOMs are likewise significant. The roles of rectus EOMs for ocular rotation via their scleral insertions, especially the highly muscular MR, are for typical supra/infraductions and nasal/temporal ductions. The palpebral bellies accentuate these ductions by translating the globe and surrounding structures in the same direction.

Cross‐sectional MRI of a melon‐headed whale shows the complete fusion of the palpebral bellies of rectus extraocular muscles (red dots) except that of the medial rectus (MR) muscle (green dots). Our results suggest that the fused palpebral bellies are mainly responsible for dorso‐ventral and naso‐temporal translation of the eye which may be unique to cetaceans. Yellow dots show the scleral belly of MR.

1. INTRODUCTION

The rectus extraocular muscles (EOMs) of mammals, and vertebrates generally, insert onto the sclera of the eye to effect ocular rotations. In addition to these scleral insertions, the four rectus EOMs in cetaceans have large, fleshy palpebral insertions that spread into the deep surface of the upper and lower eyelids (Figure 1 and see Meshida et al., 2020, 2021). The unusual cetacean palpebral rectus divisions have been known at least since the time of John Hunter's Observations on the structure and oeconomy of whales (Hunter, 1787). He described four large orbital muscles diverging from the four rectus eye muscles and inserting into the eyelids in dissections of seven species of odontocetes and mysticetes. He termed these palpebral insertions as ‘dilatores of the eyelids’ and gave functional names also to the scleral portions of the rectus muscles, calling them collectively the ‘interior straight muscles’ and separately, the ‘elevator, depressor, adductor and abductor’ muscles of the eye (Hunter, 1787). He also gave clear accounts of the oblique EOMs (Meshida et al., 2021) and the retractor bulbi muscles (Meshida et al., 2020), though without naming the latter as such. Richard Owen confirmed and clarified Hunter's results in editorial notes added to a republication of Hunter's papers (Hunter, 1840). Weber (1886) provided the next significant contribution on cetacean orbital anatomy when, after translating the relevant pages from Hunter, he described the palpebral bellies of rectus EOMs as ‘musculus palpebralis’, though confirming them as parts of the four recti. This terminology was followed by subsequent workers such as Pütter (1903), Groyer (1903) and Hosokawa (1951). The best demonstration of the palpebral attachments of the rectus EOMs in cetaceans was provided by the dissections and MRI results of Zhu et al. (2000, 2001) in their studies of arctic bowhead whales. They demonstrated an intermingling of rectus palpebral insertions with the circular fibres of the m. orbicularis oculi and concluded that the rectus fibres played a role in retracting the eyelids. We follow them in using the terms ‘palpebral belly’ or ‘palpebral insertion’ instead of ‘m. palpebralis’ for the palpebral portions of the rectus EOMs.

FIGURE 1.

Massive palpebral belly and weakly developed scleral belly of rectus EOMs in cetaceans. (a, b) SR, LR and MR in minke whale (Balaenoptera acutorostrata, USNM 593554 R) and (c) MR in pygmy sperm whale (Kogia breviceps, USNM 594027 R) demonstrate the scleral parts inserting onto the anterior hemisphere close to the equator (widest point) of the globe. (d) Scleral MR is slightly thicker than that of the other rectus EOMs in minke whale (Balaenoptera acutorostrata, USNM 504674 L), although it is not nearly as muscular as that in Odontoceti. (e, f) MRI clearly show massive palpebral belly and weaker scleral belly of rectus EOMs in sperm whale (Physeter macrocephalus, 594183 R) and in Risso's dolphin (Grampus griseus, 594001 L) respectively. Yellow dotted circles show the joint insertion of palpebral belly of rectus EOMs (SR and IR), ECM and ICM in (e). Scleral part of SR is not visible in (f); probably it is pushed against the palpebral part of SR (superior to SO in this image). Abbreviations: A, apical, toward orbital apex; CN II, optic nerve; ECM, external circular muscle (orbitalis); ICM, internal circular muscle; IO, inferior oblique; IR, inferior rectus; LR, lateral rectus; MR, medial rectus; MRI, magnetic resonance imaging; N, nasal; p, palpebral belly; ORM, ophthalmic rete mirabile; RB, retractor bulbi; s, scleral belly; SO, superior oblique; SR, superior rectus; T, temporal; V, ventral. Scale bars: 10 mm

1.1. Functions of palpebral rectus bellies

Although the unusual palpebral portions of the rectus EOMs in cetaceans have long been known, their functions remain obscure. The oldest (Hunter, 1787) and most recent works (Zhu et al., 2000, 2001) describe them as dilators or retractors of the eyelids. Both gross anatomy and observations of live cetaceans seem to support this, at least when the eyes are in their protruded positions (Meshida et al., 2020). Weber (1886) ascribed to them mechanical protection of the eyeball against water pressure during diving, but this does not appear to be a viable hypothesis given the great pressures that would be involved, and possibly, the lack of a need for this function as the orbital contents and globe are not compressible. While protection against water pressure seems unlikely, the palpebral insertions may nevertheless contribute to firm closure of the eyelids when the globe is already retracted into the orbit (see Meshida et al., 2020 for discussion of retraction/protrusion of cetacean eyes). Pütter (1903) suggested that the large masses of the palpebral muscles helped protect the eyeball and orbital contents from cooling by myogenic heat production. Thermogenic functions of rectus muscles are known in other vertebrates (Block, 1987) and large palpebral muscle bellies would likely be useful for any aquatic mammals that dwell in cold waters.

In addition to roles in opening and closing the eyelids and warming the orbital contents the present work proposes possible functions for the cetacean palpebral rectus muscles during eye movements, namely, to translate the globe in the direction of gaze changes. These dorso‐ventral and naso‐temporal translations that occur during large angle gaze changes have not received any special notice, but they are readily observable in captive animals and in video footage from the wild. Based on gross anatomy we propose that the palpebral bellies of rectus EOMs drive these translations of the eyeball while the scleral bellies directly drive rotation of the eyeball.

1.2. Global and orbital layers of mammalian EOMs

The taxonomic distribution and tissue origins of large palpebral insertions of rectus EOMs should provide clues to their emergence and elaboration within mammals. Embryological data regarding them are completely lacking thus the adult anatomy of rectus EOM insertions in different mammals provides the main evidence for their evolutionary origins. Of particular importance is the presence of both global and orbital insertions of EOMs demonstrated in humans and a variety of laboratory animals. An overview of current understanding of human EOMs and their pulley system is summarized elsewhere (Demer, 2017; Meshida et al., 2021). The globe is surrounded by a dense, elastic fibrovascular connective tissue called Tenon's capsule (fascia bulbi) which also invests the anterior (distal) portions of the EOMs (Dutton, 2011; Fink, 1962). Each EOM is surrounded by a connective tissue sleeve where it penetrates the Tenon's capsule, the sleeve serving as a ‘pulley’ which deflects the course of the muscle towards the orbital wall, thus establishing a mobile ‘functional origin’ of each EOM. The EOMs are stratified into global and orbital layers each with unique fibre types, innervation patterns and insertions (Leigh & Zee, 2016; Spencer & Porter, 1988, 2006). The global layers are rich in glycolytic twitch fibres suited to phasic activity and terminate as tendinous insertions into the sclera for driving rotation of the globe. The orbital layers of the EOMs are dominated by oxidative twitch fibres whose fatigue resistance suits them for more constant tonic activity. These fibres insert into the connective tissue pulleys thus serving to influence the pulling direction of the EOMs (Demer, 2007, 2017; Spencer & Porter, 2006). Other than human EOMs, evidence for presence of global and orbital layers of mammalian EOMs have been reported in a few domesticated and laboratory species such as cat, rabbit, rat, mouse, sheep, monkey, camel, pig and calf (Büttner‐Ennever, 2007; Lucas et al., 2018; Spencer & Porter, 1988). Although the microstructure of the global and orbital layers of those species were described by means of immunochemical or immunohistochemical analysis, anatomical descriptions of the two layers are scarce. In this study, two insertions of each EOM, global and orbital, were found in all species examined, thus this seems to be a universal characteristic of mammalian EOMs. The overall architecture of the global and orbital portions of other mammalian EOMs will be described in this study as outgroup comparisons with their counterparts in cetacean EOMs.

1.3. Goals of the present work

Previous papers in this series focussed on (1) circular orbital muscles and retractor bulbi, emphasizing their roles in protrusion and retraction of the globe (Meshida et al., 2020), and (2) oblique EOMs and their roles in torsional eye movements, with demonstration of accessory oblique attachments to bellies and tendons of the rectus EOMs that are similar topographically to the fascial connections between obliques and recti in humans (Meshida et al., 2021). The overall orbital anatomy of a few representative odontocete and mysticete species was also summarized, and numerous descriptions and images involving cetacean rectus EOMs were presented, though only peripherally to the main subjects of those papers.

The present results focus on the rectus EOMs and demonstrate the gross structure of their scleral and palpebral portions in a variety of cetaceans. Dissections and MRI will demonstrate scleral versus palpebral bellies, their divergence points, and their insertions. The medial rectus (MR) will be shown as largely distinct from the other three recti in regard to its more muscular scleral portion. Fusion of adjacent rectus palpebral bellies will be described, with patterns varying from slight fusion of the separate muscles to a nearly continuous ring at the palpebral insertions. The external palpebral surfaces overlying where the rectus palpebral bellies insert are deeply inscribed, forming grooves or furrows, especially in mysticetes. The basic patterns of major and minor palpebral grooves will be described from a variety of cetacean specimens and archival photographs. To suggest some possible functional interpretations of the rectus EOM anatomy presented here, we describe non‐controlled visual and video observations on eye movements of captive dolphins. The observed ductions and vergences were accompanied by distinct translations of the globes (supra/infra and nasal/temporal) and appeared to involve flexions of the palpebrae at their surface grooves. To gain insight into the homologies and functions of the palpebral insertions of rectus EOMs in mammals, we then compare rectus EOM insertions across a sample of terrestrial and aquatic non‐cetacean species. This limited survey tests the generality and variations in global versus orbital insertions of the rectus EOMs and tries to determine if any of the non‐cetaceans have ‘proper’ palpebral insertions comparable to those in cetaceans.

The discussion reviews these results in terms of insights into the functions of rectus EOMs in cetacean eye movements, the parallel evolution of rectus palpebral insertions in marine mammals, and possible structural and developmental homologies between aquatic palpebral bellies and the orbital layer insertions into the Tenon's capsule in mammals generally.

2. MATERIALS AND METHODS

2.1. Dissection

The orbits of 31 cetacean specimens (40 orbital specimens) and two non‐cetacean specimens were collected at the Osteopreparation Laboratory of the Museum Support Center, Smithsonian Institution, Suitland, MD (Table 1). The eyes, eye muscles and surrounding tissues were extracted from both sides (when possible), fixed initially in 10% formalin, and then transferred to 70% ethanol for long‐term preservation. The pygmy hippopotamus (Hexaprotodon liberiensis, USNM 256491) specimen was already fixed, and the orbits were not taken out of the specimen but were dissected in situ to minimize destruction of the specimen. Eighteen additional non‐cetacean head specimens (20 orbital specimens) were obtained from the Mercer County Wildlife Center, NJ; the Smithsonian National Zoological Park, Washington D.C.; and the Florida Fish and Wildlife Commission, FL, for outgroup comparisons. All the subjects perished by natural causes or were humanely euthanized by authorized organizations; no animals were acquired or sacrificed for this study. Permission to use the materials, in some cases for destructive analysis, was granted by each of the institutions listed above and in Table 1. The specimens from the National Zoo were fixed in 10% formalin after the pathological necropsies and transferred to 70% ethanol afterwards. The orbits were dissected macro‐ and microscopically and were photographed and videotaped with a Dino‐Lite (AM4115ZT), a SONY Handycam HDR‐CX405, Nikon D3400 and D610 digital cameras. The images and videos were edited in Adobe Photoshop/Premier and figure plates were assembled in Inkscape.

TABLE 1.

Species examined in this study

Catalogue #	Group	Family	Species	Common name	Side
USNM 504674	Mysticeti	Balaenopteridae	Balaenoptera acutorostrata	Minke whale	L,R
USNM 593554	Mysticeti	Balaenopteridae	Balaenoptera acutorostrata	Minke whale	R
USNM 594656	Mysticeti	Balaenopteridae	Balaenoptera acutorostrata	Minke whale	L
USNM 594182	Mysticeti	Balaenopteridae	Balaenoptera physalus	Fin whale	R
USNM 594183	Odontoceti	Physeteridae	Physeter macrocephalus	Sperm whale	R
USNM 572142	Odontoceti	Kogiidae	Kogia breviceps	Pygmy sperm whale	L,R
USNM 593969	Odontoceti	Kogiidae	Kogia breviceps	Pygmy sperm whale	R
USNM 594027	Odontoceti	Kogiidae	Kogia breviceps	Pygmy sperm whale	L,R
USNM 571927	Odontoceti	Ziphiidae	Mesoplodon densirostris	Blainville's beaked whale	L,R
USNM 550070	Odontoceti	Ziphiidae	Mesoplodon europaeus	Gervais' beaked whale	L,R
USNM 550825	Odontoceti	Ziphiidae	Mesoplodon europaeus	Gervais' beaked whale	R
USNM 594566	Odontoceti	Ziphiidae	Mesoplodon europaeus	Gervais' beaked whale	R
USNM uncatalogued	Odontoceti	Ziphiidae	Mesoplodon sp.	beaked whale sp	R
USNM 594065	Odontoceti	Monodontidae	Delphinapterus leucas	Beluga whale	L
USNM 594045	Odontoceti	Delphinidae	Globicephala macrorhynchus	Short‐finned pilot whale	R
USNM 594001	Odontoceti	Delphinidae	Grampus griseus	Risso's dolphin	R,L (MRI)
USNM 594200	Odontoceti	Delphinidae	Lagenodelphis hosei	Fraser's dolphin	L,R
USNM 571446	Odontoceti	Delphinidae	Lagenoryhnchus acutus	Atlantic white‐sided dolphin	R
USNM 550008	Odontoceti	Delphinidae	Peponocephala electra	Melon‐headed whale	R
USNM 504419	Odontoceti	Delphinidae	Stenella coeruleoalba	Striped dolphin	R
USNM 594532	Odontoceti	Delphinidae	Stenella frontalis	Atlantic spotted dolphin	L,R
USNM 594181	Odontoceti	Delphinidae	Stenella longirostris	Spinner dolphin	R
USNM 594052	Odontoceti	Delphinidae	Steno bredanensis	Rough‐toothed dolphin	R
USNM 571618	Odontoceti	Delphinidae	Tursiops truncatus	Bottlenose dolphin	R
USNM 594054	Odontoceti	Delphinidae	Tursiops truncatus	Bottlenose dolphin	R
USNM 594531	Odontoceti	Delphinidae	Tursiops truncatus	Bottlenose dolphin	R
USNM 594664	Odontoceti	Delphinidae	Tursiops truncatus	Bottlenose dolphin	L (in situ)
USNM 593411	Odontoceti	Phocoenidae	Phocoena	Harbour porpoise	R
USNM 593413	Odontoceti	Phocoenidae	Phocoena	Harbour porpoise	L,R
USNM 593568	Odontoceti	Phocoenidae	Phocoena	Harbour porpoise	R
USNM 594066	Odontoceti	Phocoenidae	Phocoenoides dalli	Dall's porpoise	R
USNM 256491	Cetartiodactyla	Hippopotamidae	Hexaprotodon liberiensis	Pygmy hippopotamus	R
USNM 602250	Carnivora	Felidae	Puma concolor	Florida panther	L
NZP 113469	Cetartiodactyla	Bovidae	Oryx dammah	Scimitar horned oryx	L
NZP 114768	Carnivora	Mustelidae	Amblonyx cinereus	Asian small‐clawed otter	R
NZP N19‐0240	Carnivora	Felidae	Neofelis nebulosa	Clouded leopard	L
NZP N19‐0246	Carnivora	Felidae	Neofelis nebulosa	Clouded leopard	R
NZP 114878	Carnivora	Felidae	Acinonyx jubatus	South African cheetah	R
NZP W20‐0053	Carnivora	Canidae	Vulpes	Red fox	R
NZP 114197	Carnivora	Herpestidae	Suricata	Slender‐tailed meerkat	R
NZP 115799	Primates	Cebidae	Pithecia	White‐faced saki monkey	R
KM001	Cetartiodactyla	Cervidae	Odocoileus virginianus	White‐tailed deer	L,R
KM016	Cetartiodactyla	Bovidae	Capra aegagrus hircus	Goat	R
KM005	Carnivora	Procyonidae	Procyon lotor	Raccoon	R
KM020	Carnivora	Mephitidae	Mephitis	Skunk	L,R
KM003	Rodentia	Sciuridae	Marmota monax	Woodchuck	R
KM009	Rodentia	Sciuridae	Sciurus carolinensis	Gray squirrel	R
KM010	Rodentia	Sciuridae	Sciurus carolinensis	Gray squirrel	L
KM018	Lagomorpha	Leporidae	Sylvilagus floridanus	Cottontail rabbit	R
MCWC#2017‐00498	Carnivora	Felidae	Lynx rufus	Bobcat	L
MEC16111	Sirenia	Trichechidae	Trichechus manatus latirostris	Florida manatee	R

Abbreviations: KM, specimens from Mercer County Wildlife Center, L, Left; MRI, magnetic resonance imaging; NJ; MEC, Florida Fish and Wildlife Commission; NZP, National Zoological Park; R, right; USNM, National Museum of Natural History.

As pointed out by Howland and Howland (2008), the whole‐body axes and planes used by human and comparative anatomists are poorly suited for comparative analysis of ocular and orbital anatomy. The differing orientations among mammals of bony orbits and orbital contents relative to the sagittal and other planes of head and trunk mean that terms such as ‘axial’, ‘frontal’ and ‘sagittal’ planes lose their usefulness. Thus, we will use terms relating to the ‘orbital axis’ running from ocular pupil to orbital apex as employed in current ophthalmological MRI studies (e.g., Demer, 2017; Demer et al., 1995). This axis is termed ‘antero‐posterior’ by Howland and complements the ‘dorso‐ventral’ and ‘naso‐temporal’ axes of orbital structures.

2.2. Magnetic resonance imaging

Orbital contents of a minke whale (Balaenoptera acutorostrata, USNM 593554 L,R) and a sperm whale (Physeter macrocephalus, USNM 594183 R) were scanned with a GE Signa HDxt 3T clinical MRI (General Electric Medical Systems, Milwaukee, WI) with a quadrature knee/foot coil (GE) at the Department of Radiology in the Howard University Hospital, Washington, D.C. Images of orbital contents of a Risso's dolphin (Grampus griseus, USNM 594001 L), a melon‐headed whale (Peponocephala electra, USNM 550008 R) and a sperm whale (USNM 594183 L) were acquired with a Bruker AVANCE III 7T research MRI (Bruker BioSpin, Billerica, MA) using a 90mm quadrature volume coil (RAPID Biomedical, Rimpar, Würzburg, Germany) at the Molecular Imaging Laboratory, Department of Radiology, Howard University College of Medicine, Washington, D.C. Anatomic scans were acquired using T1‐ and T2‐weighted 2D fast spin echo (RARE) sequences with fat suppression. T1‐weighted scans were acquired with TE = 7 ms, TR = 1750 ms, NA = 16, RARE factor = 4, 45 × 2 mm slices, FOV = 90 × 80 mm, matrix = 256 × 512 pixels. T2‐weighted scans were acquired with TE = 33 ms, TR = 5000 ms, NA = 16, RARE factor = 8, 45 × 2 mm slices, FOV = 90 × 80 mm, matrix = 256 × 512 pixels.

2.3. Photographic archival survey

In addition to the orbital specimens including undissected ones, photographic archives of the Marine Mammal Program at the Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D.C., were examined for surveying the presence/absence of the palpebral groove in different species (Table 2).

TABLE 2.

Palpebral groove variations

Catalogue #	Family	Species	Common name	Groove	Sources
USNM 504674	Balaenopteridae	Balaenoptera acutorostrata	Minke whale	Distinct	Dissection
USNM 593554	Balaenopteridae	Balaenoptera acutorostrata	Minke whale	Distinct	Dissection
USNM 504485	Balaenopteridae	Balaenopetra physalus	Fin whale	Distinct	Archives
USNM 571562	Balaenopteridae	Balaenoptera physalus	Fin whale	Distinct	Archives
USNM 594182	Balaenopteridae	Balenopetera physalus	Fin whale	Distinct	Dissection
STR 17537	Balaenopteridae	Balaenoptera physalus	Fin whale	Distinct	Archives
STR 17556	Balaenopteridae	Balaenoptera physalus	Fin whale	Distinct	Archives
USNM 20984	Balaenopteridae	Balaenoptera musculs	Blue whale	Distinct	Archives
UNSM 484991	Balaenopteridae	Megaptera novaengliae	Humpback whale	Distinct	Archives
STR 10901	NeoBalaenidae	Caperea marginata	Pygmy right whale	Positive	Archives
USNM 594183	Physeteridae	Physeter macrocephalus	Sperm whale	N/A	Dissection
USNM 504136	Kogiidie	Kogia breviceps	Pygmy sperm whale	No	Archives
USNM 504471	Kogiidie	Kogia breviceps	Pygmy sperm whale	No	Archives
USNM 571321	Kogiidie	Kogia breviceps	Pygmy sperm whale	No	Archives
USNM 572142	Kogiidie	Kogia breviceps	Pygmy sperm whale	No	Dissection
USNM 593969	Kogiidie	Kogia breviceps	Pygmy sperm whale	No	Dissection
USNM 594027	Kogiidie	Kogia breviceps	Pygmy sperm whale	No	Dissection
USNM 504222	Kogiidie	Kogia sima	Dwarf sperm whale	Weak	Archives
USNM 504312	Kogiidie	Kogia sima	Dwarf sperm whale	Weak	Dissection
USNM 504594	Kogiidie	Kogia sima	Dwarf sperm whale	No	Archives
USNM 550900	Ziphiidae	Berardius bairdii	Baird's beaked whale	Positive	Archives
USNM 571524	Ziphiidae	Berardius bairdii	Baird's beaked whale	Positive	Archives
USNM 571525	Ziphiidae	Berardius bairdii	Baird's beaked whale	Positive	Archives
USNM 571531	Ziphiidae	Berardius bairdii	Baird's beaked whale	Positive	Archives
USNM 571543	Ziphiidae	Berardius bairdii	Baird's beaked whale	Positive	Archives
USNM 571544	Ziphiidae	Berardius bairdii	Baird's beaked whale	Positive	Archives
USNM 572533	Ziphiidae	Berardius bairdii	Baird's beaked whale	Positive	Archives
USNM 504612	Ziphiidae	Mesoplocon mirus	True's beaked whale	Positive	Archives
USNM 504724	Ziphiidae	Mesoplocon mirus	True's beaked whale	Positive	Archives
USNM 594039	Ziphiidae	Mesoplocon mirus	True's beaked whale	Positive	Dissection
USNM 504756	Ziphiidae	Ziphius cavirostris	Cuvier's beaked whale	Positive	Archives
USNM 550734	Ziphiidae	Ziphius cavirostris	Cuvier's beaked whale	No	Archives
USNM 504950	Ziphiidae	Mesoplodon densirostris	Blainville's beaked whale	Positive	Archives
USNM 550338	Ziphiidae	Mesoplodon densirostris	Blainville's beaked whale	Weak	Archives
USNM 571927	Ziphiidae	Mesoplodon densirostris	Blainville's beaked whale	Weak	Dissection
USNM 594202	Ziphiidae	Mesoplodon densirostris	Blainville's beaked whale	Positive	Dissection
USNM 504256	Ziphiidae	Mesoplodon europaeus	Gervais' beaked whale	Weak	Archives
USNM 504738	Ziphiidae	Mesoplodon europaeus	Gervais' beaked whale	Positive	Archives
USNM 550069	Ziphiidae	Mesoplodon europaeus	Gervais' beaked whale	Positive	Archives
USNM 550070	Ziphiidae	Mesoplodon europaeus	Gervais' beaked whale	No	Dissection
USNM 550105	Ziphiidae	Mesoplodon europaeus	Gervais' beaked whale	Positive	Archives
USNM 550825	Ziphiidae	Mesoplodon europaeus	Gervais' beaked whale	No	Dissection
USNM 571376	Ziphiidae	Mesoplodon europaeus	Gervais' beaked whale	Positive	Archives
USNM 572520	Ziphiidae	Mesoplodon europaeus	Gervais' beaked whale	Positive	Dissection
USNM 572952	Ziphiidae	Mesoplodon europaeus	Gervais' beaked whale	Positive	Dissection
USNM 594566	Ziphiidae	Mesoplodon europaeus	Gervais' beaked whale	Positive	Dissection
USNM no number	Ziphiidae	Mesoplodon sp.	Beaked whale sp	No	Dissection
USNM 594065	Monodontidae	Delphinapterus leucas	Beluga whale	Weak	Dissection
USNM 487817	Delphinidae	Delphinus delphis	Short‐beaked common dolphin	Weak	Archives
USNM 504219	Delphinidae	Delphinus delphis	Short‐beaked common dolphin	Weak	Archives
USNM 550550	Delphinidae	Delphinus delphis	Short‐beaked common dolphin	Weak	Archives
USNM 550755	Delphinidae	Delphinus delphis	Short‐beaked common dolphin	Weak	Archives
USNM 550815	Delphinidae	Delphinus delphis	Short‐beaked common dolphin	Positive	Archives
USNM 550862	Delphinidae	Delphinus delphis	Short‐beaked common dolphin	No	Archives
USNM 550885	Delphinidae	Delphinus delphis	Short‐beaked common dolphin	No	Archives
USNM 550920	Delphinidae	Delphinus delphis	Short‐beaked common dolphin	No	Archives
USNM 550925	Delphinidae	Delphinus delphis	Short‐beaked common dolphin	Weak	Archives
USNM 571438	Delphinidae	Delphinus delphis	Short‐beaked common dolphin	No	Archives
USNM 500246	Delphinidae	Globicephala macrorhynchus	Short‐finned pilot whale	Positive	Archives
USNM 594045	Delphinidae	Globicephala macrorhynchus	Short‐finned pilot whale	Weak	Dissection
USNM 504923	Delphinidae	Globicephala melas	Long‐finned pilot whale	No	Archives
USNM 550988	Delphinidae	Globicephala melas	Long‐finned pilot whale	Weak	Archives
USNM 550990	Delphinidae	Globicephala melas	Long‐finned pilot whale	No	Archives
USNM 550437	Delphinidae	Grampus griseus	Risso's dolphin	No	Archives
USNM 594001	Delphinidae	Grampus griseus	Risso's dolphin	Weak	Dissection
USNM 504148	Delphinidae	Lagenorhynchus acutus	Atlantic white‐sided dolphin	Weak	Archives
USNM 504161	Delphinidae	Lagenorhynchus acutus	Atlantic white‐sided dolphin	Weak	Archives
USNM 571387	Delphinidae	Lagenorhynchus acutus	Atlantic white‐sided dolphin	No	Archives
USNM 571446	Delphinidae	Lagenoryhnchus acutus	Atlantic white‐sided dolphin	No	Dissection
USNM 594200	Delphinidae	Lagenodelphis hosei	Fraser's dolphin	No	Dissection
jm0354 (*)	Delphinidae	Lagenorhynchus obliquidens	Atlantic white‐sided dolphin	Weak	Archives
STR 16232	Delphinidae	Orcinus orca	Killer whale	No	Archives
USNM 504948	Delphinidae	Peponocephala electra	Melon‐headed whale	No	Archives
USNM 550008	Delphinidae	Peponocephola electra	Melon‐headed whale	Positive	Dissection
USNM 594000	Delphinidae	Pserudorca crassidens	False killer whale	N/a	Dissection
USNM 504034	Delphinidae	Stenella attenuata	Pantropical spotted dolphin	No	Foetus no dissection
USNM 571514	Delphinidae	Stenella attenuata	Pantropical spotted dolphin	Weak	Archives
USNM 504408	Delphinidae	Stenella clymene	Clymene dolphin	Positive	Archives
USNM 504086	Delphinidae	Stenenna coeruleoalba	Striped dolphin	Weak	Archives
USNM 504419	Delphinidae	Stenella coerureoalba	Striped dolphin	Weak	Dissection
USNM 571843	Delphinidae	Stenella coeruleoalba	Striped dolphin	Weak	Dissection
USNM 504321	Delphinidae	Stenella frontalis	Atlantic spotted dolphin	Weak	Archives
USNM 550751	Delphinidae	Stenella frontalis	Atlantic spotted dolphin	Weak	Archives
USNM 550800	Delphinidae	Stenella frontalis	Atlantic spotted dolphin	No	Archives
USNM 593532	Delphinidae	Stenella frontalis	Atlantic spotted dolphin	Weak	Dissection
USNM 504524	Delphinidae	Stenella longirostris	Spinner dolphin	Weak	Archives
USNM 594181	Delphinidae	Stenella longilostris	Spinner dolphin	Weak	Dissection
USNM 504487	Delphinidae	Steno bredanensis	Rough‐toothed dolphin	Positive	Archives
USNM 504492	Delphinidae	Steno bredanensis	Rough‐toothed dolphin	Positive	Archives
USNM 504497	Delphinidae	Steno bredanensis	Rough‐toothed dolphin	Positive	Archives
USNM 550368	Delphinidae	Steno bredanensis	Rough‐toothed dolphin	Positive	Archives
USNM 550369	Delphinidae	Steno bredanensis	Rough‐toothed dolphin	Positive	Archives
USNM 550371	Delphinidae	Steno bredanensis	Rough‐toothed dolphin	Positive	Archives
USNM 594052	Delphinidae	Steno bredanensis	Rough‐toothed dolphin	Weak	Dissection
USNM 504122	Delphinidae	Tursiops truncatus	Bottlenose dolphin	No	Archives
USNM 504273	Delphinidae	Tursiops truncatus	Bottlenose dolphin	Weak	Archives
USNM 571381	Delphinidae	Tursiops truncatus	Bottlenose dolphin	Weal	Archives
USNM 571385	Delphinidae	Tursiops truncatus	Bottlenose dolphin	Weak	Archives
USNM 571618	Delphinidae	Tursiops truncatus	Bottlenose dolphin	N/A	Dissection
USNM 571687	Delphinidae	Tursiops truncatus	Bottlenose dolphin	Positive	Archives
USNM 593582	Delphinidae	Tursiops truncatus	Bottlenose dolphin	Positive	No dissection
USNM 594054	Delphinidae	Tursiops truncatus	Bottlenose dolphin	N/a	Dissection
USNM 594531	Delphinidae	Tursiops truncatus	Bottlenose dolphin	N/a	Dissection
USNM 593411	Phocoenidae	Phocoena phocaena	Harbour porpoise	No	Dissection
USNM 593413	Phocoenidae	Phocoena phocaena	Harbour porpoise	No	Dissection
USNM 593568	Phocoenidae	Phocoena phocoena	Harbour porpoise	No	Dissection
USNM 594066	Phocoenidae	Phocoenoides dalli	Dall's porpoise	No	Dissection
Non cetacean specimens
USNM 256491	Hippopotamidae	Hexaprotodon liberiensis	Pygmy hippopotamus	Positive	Dissection
MEC16111	Trichechidae	Trichechus manatus latirostris	Florida manatee	No	Dissection

^*Field number (uncatalogued); N/A, not observed due to severe freezer burn.

2.4. Observation and recording of the captive dolphins

The visual and video observations of eye movements in captive bottlenose dolphins (Tursiops truncatus) were carried out at the National Aquarium in Baltimore, MD. The close‐up observation was conducted by the pool and through observation tank. The eye movement of the animals were photographed and videotaped with a SONY Handycam HDR‐CX405, Nikon D3400 and D610 digital cameras when the subjects were freely swimming and when partially out of water at their familiar pool edge locations.

3. RESULTS

3.1. Palpebral and scleral moieties of rectus EOMs

Every rectus EOM in every cetacean species examined had distinctive larger palpebral and smaller scleral portions. In no case were these portions completely separate from each other at their origins nor was either portion ever absent. Typically, the palpebral parts are muscular and fused with each other to a greater or lesser degree, forming a thick cone or sheet of muscle (see details below in ‘fused palpebral belly’ section); thus, each portion (superior, inferior, lateral and medial) is continuous with the adjacent portions. The external surface of the palpebral portion is surrounded by the external circular muscle (ECM or orbitalis muscle, see Meshida et al., 2020), forming a ‘gimbal’ together with the fused palpebral portion (Meshida et al., 2021). The scleral portion of each rectus EOM arises from the corresponding main muscle belly around the posterior hemisphere of the globe and is fibrous towards the scleral insertion, except that of MR in small to mid‐sized odontocetes (see details below in ‘muscular MR’ section).

Scleral bellies and insertions of rectus EOMs in most cetaceans are small in comparison to the palpebral ones, with thin fibrous tendons inserting into the anterior hemisphere of the globe close to the equator (widest point) of the eyeball. The insertion of the scleral belly of superior rectus (SR) is anterior (on conjunctival side) to the scleral insertion of superior oblique (SO), while that of the scleral belly of inferior rectus (IR) is posterior (on apical side) to the scleral insertion of IO (Meshida et al., 2021, figs 4 and 7). There is a tendency for the scleral bellies of rectus EOMs to be more fibrous in baleen whales than in smaller toothed whales. In a minke whale (Balaenoptera acutorostrata, USNM 593554 R), scleral bellies of all rectus EOMs are fibrous while the palpebral bellies are thick and muscular (Figure 1a). The scleral belly of MR, though fibrous, is thicker than that of other rectus EOMs, but not as muscular as that of small odontocetes (Figures 1d and 3a–c). Each belly of a palpebral rectus EOM is slightly fused with the adjacent bellies via CT towards the insertion into the palpebra.

FIGURE 3.

Muscular scleral belly of MR in small‐to‐middle‐sized toothed whales. They remain muscular throughout their course and cylindrical in shape. (a) Harbour porpoise (Phocoena phocoena, USNM 593413 L). (b) Risso's dolphin (Grampus griseus, USNM 5940010 R). (c) Atlantic spotted dolphin (Stenella frontalis, USNM 594532, L). Abbreviations: A, apical, toward orbital apex; D, dorsal; MR, medial rectus; N, nasal; p, palpebral belly; RB, retractor bulbi; s, scleral belly; T, temporal; V, ventral. Scale bars: 10 mm

In toothed whales, the scleral bellies of rectus EOMs are also fibrous and thinner compared to the palpebral bellies of the rectus muscles but are thicker than those of baleen whales. An exception is that in a pygmy sperm whale (Kogia breviceps, USNM 594027 R), all the scleral bellies including that of MR are fibrous (Figure 1c), as in baleen whales such as the fin whale (Balaenoptera physalus USNM 594182, R) and minke whale (Balaenoptera acutorostrata, USNM 504674, L). The MRIs of sperm whale (Physeter macrocephalus, USNM 594183, R) and Risso's dolphin (Grampus griseus, USNM 594001 L) show the massive palpebral insertions of SR and IR compared to the weakly developed scleral bellies of SR and IR (Figure 1e,f). The palpebral bellies of rectus EOMs in the sperm whale insert onto the eyelid together with the internal circular muscle (ICM) and external circular muscle (ECM) (circled in yellow dotted line in Figure 1e).

3.2. Fusion of palpebral rectus EOMs: Variations

The palpebral belly of each rectus except MR is fused with adjacent rectus muscles to a lesser or greater degree in cetaceans. In other aquatic mammals such as the Florida manatee (Trichechus manatus latirostris) and pygmy hippopotamus (Hexaprotodon liberiensis), palpebral bellies of rectus EOMs are weakly fused only at the insertion on the eyelid. No fusion of palpebral bellies was found in the terrestrial mammals that were examined. The types of fusions can be divided into three categories:

• Type 1) Palpebral bellies are separable into four in moderate to greater degree, and each rectus muscle is connected to the adjacent rectus palpebral bellies via connective tissue (CT).

• Type 2) Palpebral bellies are continuous except at the gap between SR and MR.

• Type 3) Palpebral muscle bellies SR, LR and IR are fused and independent of MR.

Type 1) includes both baleen whales (Balaenoptera acutorostrata, Balaenoptera physalus) and toothed whales (Kogia breviceps, Kogia sima and Physeter macrocephalus). In the minke whale (Balaenoptera acutorostrata, USNM 504674 R), the continuation of the palpebral bellies is completed via CT, yet MR is not fused with the adjacent palpebral bellies of rectus EOMs (Figure 2a, also see fig. 5b in Meshida et al., 2020). In three specimens of pygmy sperm whale (Kogia breviceps), the four bellies are connected via CT, thus Type 1. However, in two specimens (Kogia breviceps, USNM 594027 R, USNM 593969 R), there was a gap between SR and MR as in beaked whales (Mesoplodon spp.). Fusion of all recti in Type 1 specimens was stronger towards their insertions.

FIGURE 2.

Different fusion types of palpebral belies in cetaceans. Type 1: each palpebral belly of rectus EOMs is fused with adjacent counterparts as shown in (a) minke whale (Balaenoptera acutorostrata, USNM 504674 R). Type 2: palpebral rectus EOMs are fused except MR as in (b) Gervais' beaked whale (Mesoplodon europaeus, USNM 550070 R). In Type 3, MR is covered by third layer of ECM in (c) Atlantic spotted dolphin (Stenella frontalis USNM, 594532 L), (d) Stenella frontalis (USNM 594532 R) and (e) Fraser's dolphin (Lagenodelphis hosei, USNM 594200 L). MR is partially covered by palpebral belly of IR and third layer of ECM in (f–g) harbour porpoise (Phocoena phocoena, USNM 593413 L, USNM 593411 R), (h) Atlantic white‐sided dolphin (Lagenorhynchus acutus, USNM 571446 R) and (i) bottlenose dolphin (Tursiops truncatus, USNM, 594531 R). The thick CT ‘pocket’ encloses MR in (j) Atlantic spotted dolphin (Stenella frontalis, USNM 594532 R). (k, l) Fused palpebral bellies of rectus EOMs are demonstrated in the cross‐sectional MRI of melon‐headed whale (Grampus griseus, USNM 594001 L). The red line in (k) is the plane of section of (l). While MR has palpebral (red dots) and scleral (yellow) parts as in other recti, palpebral belly of MR is completely separated from the fused SR, LR and IR palpebral bellies (red dots). Abbreviations: A, apical, toward orbital apex; CN II, optic nerve; CT, connective tissue; ECM, external circular muscle (orbitalis); IO, inferior oblique; IR, inferior rectus; LR, lateral rectus; MR, medial rectus; N, nasal; RB, retractor bulbi; SO, superior oblique; SR, superior rectus; T, temporal; V, ventral. Scale bars: 10 mm

Type 2) is found in beaked whales: two Gervais' beaked whales (Mesoplodon europaeus) and one Blainville's beaked whale (Mesoplodon densirostris). The gap between SR and MR is filled with CT. This may be unique to beaked whales (Mesoplodon) (Figure 2b).

Type 3) comprises the rest of the small to medium‐sized toothed whales. The external surface of MR is covered by palpebral IR, CT and/or 3rd layer of ECM (orbitalis). In Atlantic spotted dolphin (Stenella frontalis, USNM 594532 L, R) and Fraser's dolphin (Lagenodelphis hosei, USNM 594200 L), MR is covered by the third layer of ECM (orbitalis) externally (Figure 2c–e). In harbour porpoise (Phocoena, USNM 593413 L, 593411 R), Atlantic white‐sided dolphin (Lagenorhynchus acutus, USNM 571446 R) and bottlenose dolphin (Tursiops truncatus, USNM 594531 R), the external surface of MR is covered mainly by the palpebral belly of IR, which is continuous with that of SR, by the 3rd layer of ECM (orbitalis) and partially by CT (Figure 2f–i). In some odontocete species, the scleral belly of lateral rectus (LR) is somewhat muscular compared to that of SR and IR but not as significantly as that of MR. The relatively well‐developed LR may be because of the function of LR as an antagonist to MR. In this type, the palpebral belly of MR is not fused with adjacent palpebral bellies of SR and IR and is embedded in thick connective tissue which looks like a ‘pocket’ for the muscle (Figure 2j). The fusion of the palpebral bellies of rectus EOMs except that of MR is clearly demonstrated in the cross‐sectional MRI of Risso's dolphin (Grampus griseus, USNM 594001 L) (Figure 2k,l, also see fig. 2 in Meshida et al., 2021). While the MR is massive and has its own palpebral and scleral portions like other recti, complete independence of palpebral MR from other recti is well demonstrated in the MRI.

3.3. Muscular scleral belly of medial rectus (MR) in small to mid‐sized Odontoceti

The palpebral bellies of adjacent rectus EOMs are fused together in moderate to extreme degrees in all species examined, with some exceptions in MR of some odontocete species. In some odontocetes such as Risso's dolphin (Grampus griseus), harbour porpoise (Phocoena phocoena), short‐finned pilot whale (Globicephala macrorhynchus), melon‐headed whale (Peponocephala electra), beluga whale (Delphinapterus leucas), rough‐toothed dolphin (Steno bredanensis), Dall's porpoise (Phocoenoides dalli), striped dolphin (Stenella coeruleoalba), spinner dolphin (Stenella longirostris), pantropical spotted dolphin (Stenella attenuata), Fraser's dolphin (Lagenodelphis hosei), bottlenose dolphin (Tursiops truncatus) and Atlantic white‐sided dolphin (Lagenorhynchus acutus), the scleral insertion of MR is thick and muscular until the scleral insertion point, and is cylindrical in shape. The muscular scleral belly of MR is particularly prominent in the harbour porpoise (Phocoena, USNM 593413 L), Risso's dolphin (Grampus griseus, USNM 594001 R) and Atlantic spotted dolphin (Stenella frontalis, USNM 594532 L) (Figure 3a–c). In contrast, there is a tendency for larger odontocetes and mysticetes such as pygmy sperm whale (Kogia breviceps, Figure 1c), Gervais' beaked whale (Mesoplodon europaeus), Blainville's beaked whale (Mesoplodon densirostris), sperm whale (Physeter macrocephalus) (Odontoceti), minke whale (Balaenoptera acutorostrata, Figure 1a,b,d) and fin whale (Balaenoptera physalus) (Mysticeti) to have flat, less muscular or even fibrous scleral bellies of MR as described above.

The species with a muscular scleral belly of MR correspond to Type 3 in fusion of rectus EOMs. The majority of the species in this group spend most of their lives above 100 m in water depth (Mead & Gold, 2002). Although some species such as the short‐finned pilot whale (Globicephala macrorhynchus) are capable of diving to depths of nearly 1000 m, they also spend significant amounts of time at the surface (Alves et al., 2013). Compared to other deep‐diving species such as the pygmy sperm whale (Kogia breviceps), beaked whales (Mesoplodon spp.) and sperm whale (Physeter macrocephalus), the small to mid‐sized species inhabit shallower waters where they can utilize their vision more than those that spend most of their time in deep water which has dim light. Direct observation of the eye movements of captive bottlenose dolphins (Tursiops truncatus) also has proven that they use frontal vision, which requires the action of the scleral belly of MR for convergence of the eyes.

In the minke whale (Balaenoptera acutorostrata), fin whale (Balaenoptera physalus), pygmy sperm whale (Kogia breviceps), Gervais' beaked whale (Mesoplodon europaeus), Blainville's beaked whale (Mesoplodon densirostris) and sperm whale (Physeter macrocephalus), the main MR muscle belly itself is thick, although the fusion of the palpebral belly of MR to the adjacent recti (SR and IR) is moderate (Type 1 fusion). In these groups the scleral belly of MR is thicker than that of other rectus EOMs, yet not as muscular as that of the small to mid‐sized odontocetes described above (Figures 1c,d and 3a–c). This suggests that the force of converging the eyes by MR may be stronger in small to mid‐sized odontocetes that possess massive palpebral and scleral MR than in Type 1 and 2 groups described above. In addition, the palpebral belly of MR in the small to mid‐sized odontocetes is completely independent from the adjacent palpebral bellies of rectus EOMs (SR and IR), which can give more flexibility and a wider range of movement of MR in these groups.

3.4. Palpebral grooves (furrows) in cetaceans: Flexible articulations?

It is also important to note that most cetaceans have palpebral grooves/furrows on the dorsal and ventral sides of the eyelid. They are particularly distinct in mysticeti running along the length of the palpebral fissure. Some odontocei also possess the grooves although they are less prominent than those in mysticeti, with exception of those in adult sperm whales. They are called dorsal and ventral grooves (Berta et al., 2015; Rodrigues et al., 2015) or furrows (Carte et al., 1868; Zhu et al., 2001; Buono et al., 2012) yet their function is not described in any of the literatures. Mysticeti and sperm whales possess additional multiple grooves on both dorsal and ventral surface of the eyelids which are shorter and less prominent than the main ones (Figure 4). In this study, we call the main and additional ones as the palpebral grooves and the accessory palpebral grooves respectively. Our observation of the palpebral grooves in different species will be described below together with the Table 2.

FIGURE 4.

Palpebral grooves found in the external surface of the eyelid in cetaceans. Mysticetes such as (a) minke whale (Balaenoptera acutorostrata, USNM 593554 R) and (b) fin whale (Balaenoptera physalus, USNM 594182 L) have prominent main grooves (yellow arrows) on dorsal and ventral eyelids, each with multiple accessory grooves (light blue arrows). In contrast, odontocetes such as (c) bottlenose dolphin (Tursiops truncatus USNM 593582 R) exhibits less developed main groove on each side.  Abbreviations: N, nasal; T, temporal; V, ventral. Scale bars: 10 mm

All mysticete specimens directly examined as well as in the photographic archive (Marine Mammal Program, Smithsonian National Museum of Natural History: minke whale: Balaenoptera acutorostrata, blue whale: Balaenoptera musculus, fin whale: Balaenoptera physalus, humpback whale: Megaptera novaeangliae, pygmy right whale: Caperea marginata) have distinct and deep palpebral grooves (Table 2). They consist of a main groove on the dorsal eyelid and one on the ventral eyelid along with accessory grooves as shown in minke whale (Balaenoptera acutorostrata, USNM 593554 R) and fin whale (Balaenoptera physalus, USNM 594182 L) (Figure 4a,b). The depth of the main palpebral groove is 12 mm (ventral) and 10 mm (dorsal) in a juvenile minke whale (Balaenoptera acutorostrata, USNM 593554 R), and 10 mm (ventral) and 8 mm (dorsal) in a juvenile fin whale (Balaenoptera physalus, USNM 594182 L). In contrast to mysticetes, the palpebral grooves in odontocetes are less prominent. They are relatively distinct in the specimens of bottlenose dolphin (Tursiops truncatus, USNM 593582 R; Figure 4c) and melon‐headed whale (Peponocephala electra, not shown), although their depth is very shallow (<1 mm).

In other odontocete specimens directly examined, the palpebral grooves were not well developed, such as in short‐finned pilot whale (Globicephala macrorhynchus, USNM 594045 R), rough‐toothed dolphin (Steno bredanensis, USNM 594052 R), beluga whale (Delphinapterus leucas, USNM 594065 L), Risso's dolphin (Grampus griseus, USNM 594001 L,R), striped dolphin (Stenella coeruleoalba, USNM 504119 R), Atlantic spotted dolphin (Stenella frontalis, USNM 593532 L,R), dwarf sperm whale (Kogia sima, USNM 504312), spinner dolphin (Stenella longirostris, USNM 594181 R), Blainville's beaked whale (Mesoplodon densirostris, USNM 571927 L,R) and Gervais' beaked whale (Mesoplodon europaeus, USNM 550070 L,R; 550825 R; 594566 R). Although the juvenile sperm whale (Physeter macrocephalus, USNM 594183) did not exhibit palpebral grooves due to severe freezer burn on the skin, it is clear that sperm whales have distinct palpebral grooves dorso‐ventrally that are visible in various media resources and literature such as Folkens et al. (2002). In the pygmy sperm whale (Kogia breviceps), harbour porpoise (Phocoena phocoena), Atlantic white‐sided dolphin (Lagenorhynchus acutus), and Fraser's dolphin (Lagenodelphis hosei), palpebral grooves were not positively identified either in the specimens or in the photographic archives.

3.5. Translation and rotation of the eyeball and translation of the centre of the eye in dolphins

The visual observations document not only that the eyeball rotates when the subjects attend to visual objects at different positions around their more or less stable head (stable for brief periods of time, 2–10 s), but also that the soft tissue surrounding the eye shifted dorso‐ventrally and naso‐temporally (Supplement video 1). The eyelids and the associated orbital structures protruded and turned in conjunction with the rotation of the eyeball when the gaze shifted to more dorsal, ventral, nasal or temporal directions. Similar eye and palpebral region movements were observed both when the subjects were freely swimming and when partially out of water at their familiar pool edge locations. Review of video footage of other captive and wild cetaceans and comparison of their extraocular anatomy confirmed that the massive palpebral bellies and insertions of the rectus EOMs of cetaceans are responsible for moving the entire palpebral region during large changes in gaze (Supplement video 1). The rapid and controlled protrusion and retraction of the eyeball seen during the movement of the orbital region suggests that these gaze changes require synchronized actions of the ECM (or orbitalis, Meshida et al., 2020) smooth muscle, RB and the four palpebral portions of the rectus EOMs (skeletal/striated muscles). Regulation of blood flow and pressure in the orbital retia and veins may also contribute to these large translations of eye position. The RB and ECM (or orbitalis) are responsible for the translation of the visual axis (translation of the eyeball), while the scleral bellies of rectus muscles play the role of rotating the eyeball. The translation of the centre of the eye and visual axis seems to involve a combination of the palpebral bellies of rectus EOMs, RB and ECMs (orbitalis). For instance when the animal looks at a posterodorsally placed object, the ECM (orbitalis) protrudes the eyeball (translation of the visual axis, horizontal translation of the eyeball, coronal plane), the palpebral belly of SR elevates the eyeball (translation of the centre of the eye, vertical translation of the eyeball, sagittal plane), and the scleral bellies of rectus muscles rotate the eyeball (rotation). When the eyeball is pulled back into the orbit, the palpebral belly of SR relaxes (translation of the centre of the eye), the scleral belly of SR relaxes (rotation), palpebral belly of the IR pulls back down (translation of the centre of the eye), and RB retracts the eyeball (translation of the eyeball).

3.6. Global and orbital insertions of rectus EOMs in non‐cetacean mammals

3.6.1. Terrestrial mammals

Two insertions were found in each rectus EOM in all terrestrial mammal specimens examined: inner and outer portions inserting onto the sclera and onto the connective tissue that surround the external surface of the EOMs respectively. The connective tissue‐like outer portions of rectus EOMs arise from the muscular main muscle belly in either the posterior hemisphere or close to the posterior pole of the eyeball. The inner part is continuous with the main muscle belly and becomes fibrous towards the scleral insertion (Figure 5a–l, inner and outer part of rectus EOMs correspond to g: global layer and o: orbital layer respectively). This pattern of the occurrence of the two portions of each rectus EOM was shared in all the terrestrial mammals examined. The two insertions of rectus EOMs are well demonstrated in Figure 5. Continuity of the outer part (‘o: orbital layer’) of rectus EOMs to the Tenon's capsule (Tc) was partially preserved in some specimens (Figure 5a,f–j) although most of them were severed in order to dissect deeper structures in other specimens. The scleral insertions were found in the anterior hemisphere or equator (widest point) of the eyeball in most terrestrial specimens examined (Figure 5a–i,k), with some variations: in cottontail rabbit, the SR inner portion inserts onto the anterior hemisphere while the rest of the rectus EOMs insert onto the equator of the eyeball (not shown). In white‐faced saki, the inner parts of the SR and IR insert around the equator of the globe while those of LR and MR insert slightly posterior to that of the SR and IR (Figure 5j). In Florida panther, the inner portions of SR and LR insert onto the equator of the eyeball while those of IR and MR insert slightly posterior to those of SR and LR (Figure 5l, LR not shown). In all non‐cetacean specimens examined, the inner part of SR tends to insert onto the sclera more anteriorly relative to the rest of the rectus EOM counterparts. The outer part of each rectus EOM in the terrestrial mammals examined inserts onto the connective tissue layer that corresponds to the Tenon's capsule, while the palpebral part of rectus EOMs inserts onto the eyelid directly in cetaceans, Florida manatee and pygmy hippopotamus (see below). Hence the inner and outer insertions of the EOMs of the terrestrial mammals examined correspond to the global and orbital layers of rectus EOMs in humans and other mammals described by Demer et al. (1997) and Oh et al. (2001) respectively.

FIGURE 5.

Two insertions of rectus EOMs in terrestrial mammals. Inner portion inserts onto the sclera while the outer part is continuous with the connective tissue layer corresponding to Tenon's capsule (T) in human orbit. Inner and outer portions of EOMs in the figures correspond to the global (g) and orbital layer (o) in human EOMs respectively. Tenon's capsule was sacrificed in deep dissections and was not preserved except in (a), (f), (g), (i), (j) and (k). The continuity of the outer portion (o) with the Tenon's capsule are well exhibited in (a), (f) and (g). (a) Bobcat MR (Lynx rufus, MCWC#2017‐00498 L), (b) raccoon LR (Procyon lotor, KM005 R), (c) grey squirrel LR (Sciurus carolinensis, KM010 L), (d) woodchuck LR (Marmota monax, KM003 R), (e) white‐tailed deer IR (Odocoileus virginianus, KM001 R), (f) red fox LR (Vulpes vulpes, NZP W020‐0053 R), (g) clouded leopard IR (Neofelis nebulosa, NZP N19‐0240 L), (h) slender‐tailed meerkat SR (Suricata suricata, NZP114197 R), (i) scimitar‐horned oryx SR (Oryx dammah, NZP113469 L), (j) white‐faced saki MR and IR (Pithecia pithecia, NZP115799 R), (k) red fox MR (Vulpes vulpes, NZP W020‐0053 R, close‐up) and (l) Florida panther SR (Puma concolor, USNM 602250 L).  Abbreviations: A, apical, toward orbital apex; CN II, optic nerve; CN III, oculomotor nerve; CN V, trigeminal nerve (maxillary division); D, dorsal; g, global layer; IO, inferior oblique; IR, inferior rectus; LPS, levator palpebrae superioris; LR, lateral rectus; MR, medial rectus; N, nasal; o, orbital layer; RB, retractor bulbi; SO, superior oblique; SR, superior rectus; T, temporal; Tc, Tenon’s capsule. Scale bars (a–j, l): 10 mm, (k): 5 mm

3.6.2. Aquatic mammals

In an apparent parallel development, the scleral insertions in a Florida manatee (Trichechus manatus latirostris, MEC16111 R) were weakly developed except for IR, and most of each rectus EOM consists of the palpebral portion (Figure 6a). The palpebral bellies are separate, although they merge towards the insertion onto the eyelid. Muscle fibres are clear in the palpebral bellies, which is opposite to what Motais (1887) described. The inner insertion of SR arises from the main muscle belly around the posterior hemisphere or posterior pole of the eyeball, while those of the rest of rectus EOMs arise near the apex of the orbit. The tendinous inner parts of the rectus EOMs insert onto the anterior hemisphere (SR and LR) or closer to the equator (MR and IR). The IR scleral insertion is much wider (7 mm) than that of other recti (2 mm) (Figure 6b). This suggests that rectus EOMs in Florida manatees have reduced function in eyeball movements, except downward movement by the relatively broad scleral belly of IR.

FIGURE 6.

Two bellies of rectus EOMs in aquatic mammals. (a, b) Massive palpebral belly and fibrous scleral belly of SR in Florida manatee (Trichechus manatus latirostris, MEC 16111 R). (b) scleral IR is wider than that of other recti in the same specimen. Palpebral IR was severed in order to show the scleral IR. (c) SR in pygmy hippopotamus (Hexaprotodon liberiensis, USNM 256491 R) has its own palpebral belly (palpebral SR was severed to show the scleral SR) while (d) palpebral belly of LR and IR merge and form one belly towards the eyelid insertion. (e, f), Two insertions of MR and SR, respectively, in the Asian small‐clawed otter (Amblonyx cinereus, NZP 114768 R). Outer portions insert onto the connective tissue layer (Tenon's capsule, not shown) as in the terrestrial mammals examined.   Abbreviations: A, apical, toward orbital apex; g, global layer; IR, inferior rectus; LPS, levator palpebrae superioris; LR, lateral rectus; MR, medial rectus; N, nasal; o, orbital layer; p, palpebral belly; s, scleral belly; SO, superior oblique; SR, superior rectus; t, trochlea; V, ventral. Scale bars (a–d): 10 mm, (e, f): 5 mm

In the pygmy hippopotamus (Hexaprotodon liberiensis, USNM 256491 R), each scleral part inserts into the sclera separately (Figure 6c). In contrast, the palpebral portions of LR and IR merge towards the palpebral insertion and become muscular and broad at the insertion (Figure 6d). The SR has its own palpebral belly, which is fibrous towards the apex and becomes muscular and wider at the insertion (Figure 6d). The palpebral belly of MR arises from the medial side of the palpebral SR and does not insert into the eyelid directly. Instead, it blends with the conjunctiva and ECM via CT which is continuous with the eyelid.

Although categorized as a semi‐aquatic animal like the pygmy hippopotamus, the Asian small‐clawed otter examined (Amblonyx cinereus, NZP 114768 R) does not have muscular palpebral bellies of rectus EOMs as in cetaceans. Each rectus EOM has two insertions, although the outer portions blend with the connective tissue corresponding to Tenon's capsule in humans. This arrangement of the outer layers resembles those of the terrestrial mammals described in the previous section. The outer parts of rectus EOMs arise from the main muscle belly in the posterior hemisphere (Figure 6e,f). The inner portions of rectus EOMs are continuous with the main muscle belly and insert onto the anterior hemisphere of the eyeball, with SR inserting more anteriorly than the rest of the rectus EOMs. Weber (1886), on the other hand, found that the Hippopotamidae did not have the palpebral belly (Mm. palpebralis), whereas the river otter did, which is opposite to our results.

4. DISCUSSION

The rectus EOMs of cetaceans conform to a common plan, with all species examined in this study possessing four recti with typical origins at the orbital apex (when observable) giving rise to ‘scleral’ bellies with tendinous insertions to the anterior hemisphere of the globe and ‘palpebral’ bellies with broad muscular insertions into the eyelids. The MR scleral insertions in some small odontocetes (Figure 3) were notably more muscular than those of the other recti and likely correlate with powerful nasalward ductions and enhanced frontal visual abilities (e.g., search ‘beluga whale’ on YouTube). The cetacean scleral bellies and insertions appear rather small in comparison to the palpebral ones (Figure 1) but compared to non‐cetaceans with large globes they are quite substantial and rather typical (see Video S1 in Meshida et al., 2021; cf. cattle and horse in Motais, 1887; Prince et al., 1960). Quantitative comparison of EOM bellies and insertions across large cetartiodactyls will be needed to access whether cetacean global EOM insertions are typical for the group or are instead either reduced or enlarged. Informal behavioural observations show typical dorso‐ventral and naso‐temporal rotations of the eye that likely result from the four scleral rectus insertions as in other vertebrates. Biomechanics of rectus actions are complicated by their functional origins from the deep surfaces of the palpebral bellies (Figure 1) as well as their attachments with the oblique muscles (see figs 6–8 in Meshida et al., 2021). Oculorotory actions of the rectus scleral insertions are complemented by the oblique EOMs (SO, IO) which generally have stout, muscular insertions related to ocular counter‐rolling for up‐down head movements (Meshida et al., 2021).

In contrast to the familiar rotatory functions of the scleral insertions of cetacean recti, their palpebral bellies and insertions may have multiple functions related not only to eyelid movements and thermoregulation, but also to non‐rotational, that is translational movements of the eyes. The rectus palpebral muscle bellies increased in width peripherally and often fused together as they reached the anterior orbit and entered palpebral connective tissues (Figure 3). Determining the mechanical consequences of different fusion patterns will require more studies of in situ orbits and eyelids to see if the fused and independent portions in different species match with differences in orbital geometry and palpebral structure. The dorsal (SR) and ventral (IR) palpebral bellies were broader than the MR and LR and appear able to exert force throughout the upper and lower eyelids respectively.

Comparison of cetacean rectus insertions with those of a variety of aquatic and terrestrial mammals showed that the palpebral portions of rectus EOMs in cetaceans are unusual but not unique among mammals. Our dissections showed that (1) all mammals examined had outer and inner portions of each rectus muscle, tentatively identified as being the orbital and global layers demonstrated in histological studies (Demer, 2017; Spencer & Porter, 1988), and (2) fused muscular outer portions of rectus EOMs that insert directly onto the eyelids are peculiar in our samples to cetaceans, pygmy hippopotamus and Florida manatee. These species are adapted to aquatic environments, the former two belonging to Cetartiodactyla and the manatee being distantly related, closer to elephants. The outer layers of rectus EOMs in terrestrial relatives of these groups insert onto the Tenon's capsule, not onto the eyelid, leading us to hypothesize that ‘palpebral’ extensions of rectus muscles have arisen more than once in relation to assumption of aquatic lifestyles by mammals. As discussed below, descriptions in the literature show even more variation in occurrence of rectus/palpebral extensions and suggest that this is a surprisingly malleable part of mammalian orbital anatomy. Finally, we will discuss two very non‐traditional functions of the cetacean rectus EOMs, translation of the eyeball during rotational eye movements and warming the orbit.

4.1. Function of palpebral EOMs and phylogenetic trait hypothesis

Based on direct observation of the eye movements of multiple captive individuals of bottlenose dolphins (Tursiops truncatus), it is clear that the animals do not just rotate the eyeballs but also move the entire orbital region (translational movement) when they follow objects with large gaze shifts. This suggests that the insertions of the palpebral bellies of the rectus EOMs into the eyelids are responsible for moving the eyelids and globe in the direction of gaze. It is important to note that the cetaceans also protrude the eyeball substantially when they move the orbital region. This suggests possible synchronized activity of rectus EOMs (skeletal/striated muscle) and ECM (orbitalis, smooth muscle, except in the sperm whale; Meshida et al., 2020).

The palpebral belly is distinctive in all cetaceans and other aquatic mammals examined. The fusion of palpebral bellies of rectus EOMs is complete or nearly complete in all cetaceans, while it is incomplete in the pygmy hippopotamus (Hexaprotodon liberiensis) and absent in the white‐tailed deer (Odocoileus virginianus) and goat (Capra aegagrus hircus). Gratiolet (1867) described the arrangement of the rectus muscles in Hippopotamus as ‘usual except MR’, and his description does not agree with the results of the pygmy hippopotamus in this study which exhibits partially fused palpebral bellies of rectus EOMs. Recent molecular and morphological phylogenetic analyses indicate that Cetacea and Hippopotamidae fall within Cetartiodactyla (Geisler & Uhen, 2003, 2005; Geisler et al., 2007; Uhen 2007). Cervidae (white‐tailed deer, Odocoileus virginianus) and Bovidae (Goat, Capra aegagrus hircus) examined in this study also belong to Cetartiodactyla. This indicates that the palpebral bellies of rectus EOMs are a shared characteristic that is unique to the aquatic Cetartiodactyla, and that Hippopotamidae display a transitional state between the fully terrestrial and aquatic Cetartiodactyla. However, the Florida manatee (Trichechus manatus latirostris) also possesses incompletely fused palpebral bellies of rectus EOMs. Since Cetacea and Sirenia are only remotely related (Sirenia belongs to Tethytheria together with Proboscidea (elephants)), the presence of the palpebral belly in the Florida manatee is a homoplasy of that of Cetacea as a result of convergent evolution and may be an adaptation to a fully aquatic lifestyle.

Although we lack data on pinnipeds and have not found any recent studies, Rosenthal (1825) illustrated palpebral extensions of rectus EOMs in harbour seal (Phoca vitulina) with slight fusion of the palpebral bellies near their insertions to the eyelids. He referred to them as four straight muscles (geraden Muskeln) with two insertions (scleral and palpebral) for each muscle belly. Weber (1886) called the scleral portions rectus muscles (Mm. recti) and the palpebral bellies, palpebralis muscles (Mm. Palpebralis). The presence of these features in pinnipeds is evidence of further parallelism since cetaceans and manatees are not at all closely related to pinnipeds.

The terrestrial specimens examined did not possess palpebral bellies; instead, they had a orbital portions that inserted onto the Tenon's capsule as in the rectus EOMs of humans and other terrestrial mammals described by Demer et al. (1997), Demer (2007, 2017) and Oh et al. (2001).

4.2. Translation and rotation of the eye in cetaceans and other mammals

In many mammals, the most significant translation of the eyeball is protrusion and retraction along an axis that runs approximately from the pupil to the orbital apex, namely, the antero‐posterior or orbital axis (Howland & Howland, 2008) Thus, the centre of the globe roughly maintains its horizontal and vertical position during both ocular rotations and protrusion/retractions. Much more than in other mammals, however, cetacean eyes can also translate horizontally in naso‐temporal directions and vertically in dorso‐ventral directions, these movements likely being mediated by the palpebral bellies of the rectus EOMs.

Translation of the globe occurs in human as well although the degree of the displacement is slight compared to that in cetaceans. During blinking, the eyeballs in humans have been shown to retract into the orbits by about a millimetre during eyelid closure due to actions of the rectus muscles (Evinger et al., 1984). More intriguingly, globe translations during horizontal eye rotation were discovered in recent MRI experiments in humans (Demer & Clark, 2019). By determining the rotational centre of the globe during rotation from abduction to adduction they were able to show that antero‐posterior and lateral translations of about a millimetre occur between far‐right and far‐left gaze. A further functional parallel exists between humans and cetaceans during upward gaze changes. During dorsal ductions in cetaceans, rotation of the eye is accompanied by dorsal movement of the globe and upper eyelid, hypothesized here to result from contraction of the SR palpebral insertion. Similar coordinated globe/lid movements occur in humans during elevation of gaze when LPS and SR work together to further raise the upper eyelid when the globe rotates in supraduction (Evinger et al., 1991).

Restriction of ocular translation within the orbit to fairly small movements seems highly desirable in mammals with retinal foveae, that is humans and other simian primates. This may not hold for most mammals, which not only lack foveae but also have ‘open’ orbits with limited bony walls. Thus, although substantial vertical and horizontal translations of the eyeball may be most obvious in cetaceans, such movements may be common among mammals. It seems likely that large globe translations are acceptable and possibly desirable in mammals with open orbits and visual streaks or other types of afoveate retinae. Possible advantages to greater mobility of the globe are the increased visual field allowed by protrusion and translation in the direction of gaze shifts and the ability for greater displacement of the globe during protective reflexes.

Since the eyes seem likely to be protruded during visual tasks in most mammals and since protrusion in many mammals is mediated as in cetaceans by the orbitalis smooth muscles, it appears that the translations and rotations of the eyeball mediating vision involve constant coordination of both striated (skeletal) and smooth muscles in the orbit as proposed for cetaceans (Meshida et al., 2020).

4.3. Palpebral grooves act as flexible hinges to increase eyelid mobility for vision and protection

This study also suggests that the translation and rotation of the eye are accommodated by the palpebral grooves on the dorsal and ventral eyelids of cetaceans. The palpebral grooves in some species appear to function as ‘accordion bellows’, providing more flexibility in movement of the eyeball and the external palpebral region, particularly when the eyeball is protruded. This indicates that the combination of function of the massive palpebral bellies of the rectus muscles, the ECM (orbitalis), and the palpebral grooves on the eyelid are all involved in moving the entire orbital region in cetaceans. Also, the dorso‐ventrally located palpebral grooves provide additional flexibility for upward‐downward movement of the eyeball facilitated by SO and IO, which supports our hypothesis that oblique muscles are mainly responsible for moving the eyeball (incyclotorsion and excyclotorsion, or inward rotation and outward rotation) together with the fused palpebral rectus EOMs (Meshida et al., 2021).

In particular, baleen whales such as the minke whale (Balaenoptera acutorostrata) and the fin whale (Balaenoptera physalus) have distinctive multiple deep palpebral grooves on the dorsal and ventral orbital region. This indicates that they have more room for movement and protrusion of the eyeball than other cetaceans, which have less distinct grooves.

Mysticetes such as the minke whale and fin whale generally spend most of their life in ‘shallower’ water (<100 m in depth), suggesting that they utilize their vision more than deep‐diving odontocetes (e.g. sperm whales and beaked whales). They also have a less muscular scleral belly of MR compared to small to mid‐sized odontocetes that spend significant amounts of time in ‘shallower’ water. The multiple deep palpebral grooves on the dorsal and ventral eyelids in mysticetes may be an adaptation for better frontal vision, providing more room for movement and protrusion of the eyeball as a compensation for a weaker MR compared to those in smaller species.

In some odontocete species examined, such as the pygmy sperm whale (Kogia breviceps), the dwarf sperm whale (Kogia sima), the harbour porpoise (Phocoena phocoena), the Atlantic white‐sided dolphin (Lagenorhynchus acutus) and the Fraser's dolphin (Lagenodelphis hosei), the palpebral grooves on the eyelids are indistinct or absent. This suggests that the range of movement of the orbital region in these species is not as large as in those with distinct palpebral grooves. The former two species are deep divers which are likely to depend less on vision. The latter three species are ‘shallow’ divers with strong scleral bellies of MR for adduction of the eyeball for frontal vision. Small to mid‐sized odontocetes may need less protrusion of the eyeball since they have smaller and more slender rostra than those of mysticetes. Hence, odontocetes, except some species such as the sperm whale, may have indistinct palpebral grooves due to less need of protrusion of the eyeball compared to mysticetes.

4.4. Possible heat‐producing function of palpebral bellies of rectus EOMs

In addition to moving the eyelids, and with them the globe, the functions of the massive palpebral bellies of rectus EOMs may include production of heat for protecting the eye from cooling, as originally suggested by Pütter (1903). Non‐oculomotor specializations of rectus EOMs are not evident in mammals but are present among fishes and include eye muscles modified for electromotor (Bennett & Pappas, 1983) as well as thermogenic functions (Block, 1986). Thermo‐regulation mechanisms involving EOMs are best known in some species of large predatory marine billfishes where heater cells derived from the SR are specialized for generating heat but not for contracting (Block, 1986). Studies on isolated swordfish retinae show that temperature elevation by orbital heating should directly result in improved visual performance (Fritsches et al., 2005). Other marine fish employ parts of the LR (butterfly mackerel) or fused portions of all four rectus EOMs (Allothunnus fallai, a basal tuna) for thermogenesis (Sepulveda et al., 2007). In the latter, a mass of EOM‐derived tissue in direct contact with the braincase but lacking contractile proteins contains an extensive vascular countercurrent system and is hypothesized to generate heat for the brain and eyes (Sepulveda et al., 2007). Some large marine sharks like Mako and Porbeagle heat the eye and brain by employing orbital vascular heat exchangers (rete mirabile) supplied not by EOMs but by red swimming muscles (Block & Carey, 1985; Wolf et al., 1988).

The possible function of heat generation by rectus EOMs in cetaceans is supported by the high degree of vascularization of the EOMs and the presence of perforating vessels joining the EOMs and ophthalmic retia mirabilia. Ninomiya et al. (2014) studied the ophthalmic rete of bottlenose dolphins and used thermography to directly demonstrate conservation of orbital heat leading them to support thermoregulatory roles for both counter‐current heat exchange and massive muscular eyelids. Additional undescribed vascular networks in the CT layer between RB and rectus EOMs in cetaceans may add additional capacity for warming the retina and optic nerve. These vascular networks were consistently found in cetacean orbits during our dissections as well as in MRIs and will be described in detail in a following article. Although the presence of specialized myogenic heat‐producing mechanisms in cetaceans has never been reported, the well‐developed ophthalmic retia and the massive palpebral bellies of recti may combine to warm the eyes for facilitating vision in cold environments.

5. CONCLUSIONS

The rectus EOMs of cetaceans are highly derived, structurally complex, multifunctional muscles. Based on gross structure they appear to participate in ocular rotation, ocular translation, palpebral dilation (and perhaps constriction) and orbital insulation/heating. The roles in ocular rotation of the SR, IR and LR scleral insertions appear secondary to actions of the more muscular oblique EOMs (counter‐rolling) and MR (frontal duction/vergence). The deep, open orbits of cetaceans allow considerable freedom of movement to the globe, thus ocular translation along axial/apical, dorso/ventral and naso/temporal axes are much greater than in humans. Unfortunately, we do not have any quantitative data regarding the range of these translations in cetaceans or any other open‐orbited mammal. Likewise, it is not clear what the effect of such translations would be for visual behaviours in afoveate mammals. Nevertheless, it appears clear that the palpebral bellies of rectus EOMs collaborate with the RB and ECM (orbitalis) muscles in translating the eyeball through a considerable volume of positions in cetaceans. It seems possible that ocular protrusion and translation in afoveate mammals expands the limits of the visual field both around the contours of the body and in the direction of rotational gaze changes. In that sense these movements are akin to head/neck rotations that accompany ipsilateral gaze shifts in humans (Leigh & Zee, 2016).

Palpebral extensions of the rectus EOMs have a variegated taxonomic distribution in mammalian lineages that include aquatic and semi‐aquatic members. This suggests separate, non‐homologous originations of these features and may indicate that insulation and heat production are the original functions of these analogous structures since thermoregulation of orbital structures would seem critical in many aquatic environments while ocular behaviour seems more diverse. A plausible hypothesis is that the cetacean palpebral muscles (and similar analogs) are hypertrophic derivatives of the orbital layer of the rectus EOMs that provide greater mobility and insulation to the eyelids in aquatic environments. In some cases, as in cetaceans, these muscles provide more controlled vertical and horizontal translations of the globe, possibly aiding in visual performance.

CONFLICTS OF INTEREST

The authors declare no conflicts of interest.

AUTHORS' CONTRIBUTIONS

Keiko Meshida involved in concept/design, acquisition of data, data analysis/interpretation, drafting and critical revision of the manuscript. Stephen Lin carried out acquisition of data (MRI), data analysis/interpretation, and critical revision of the manuscript. Daryl P. Domning and Joy S. Reidenberg carried out critical revision of the manuscript. Paul Wang carried out acquisition of data (MRI), data analysis/interpretation and critical revision of the manuscript. Edwin Gilland involved in concept/design, data analysis/interpretation, drafting, critical revision, and approval of the manuscript.

DISCLAIMER

The contents of this presentation are the sole responsibility of the author(s) and do not necessarily reflect the views, opinions or policies of Uniformed Services University of the Health Sciences (USUHS), The Henry M. Jackson Foundation for the Advancement of Military Medicine, Inc., the Department of Defense (DoD) or the Departments of the Army, Navy, or Air Force. Mention of trade names, commercial products, or organizations does not imply endorsement by the U.S. Government.

Supporting information

Video S1

Meshida, K. , Lin, S. , Domning, D.P. , Reidenberg, J.S. , Wang, P.C. & Gilland, E. (2022) The unique rectus extraocular muscles of cetaceans: Homologies and possible functions. Journal of Anatomy, 240, 1075–1094. Available from: 10.1111/joa.13628

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from the corresponding author upon reasonable request.